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1 From the Department of Clinical Nutrition, University of Kuopio, Kuopio, Finland (KSJ and HMM); the Departments of Medicine (DEL and LKN) and Clinical Chemistry (KES), Kuopio University Hospital, Kuopio, Finland; VTT Biotechnology, Espoo, Finland (KA, K-HL, and KSP);and the Department of Medical Physiology, University of Copenhagen (JJH).
2 Supported by Fazer Bakeries Ltd, Raisio Ltd, Vaasan & Vaasan Oy, Viljava Ltd, and the Technology Development Center of Finland (Tekes). 3 Address reprint requests to KS Juntunen, Department of Clinical Nutrition, University of Kuopio, PO Box 1627, 70211 Kuopio, Finland. E-mail: katri.juntunen{at}uku.fi.
ABSTRACT
Background: Rye bread has a beneficial effect on the postprandial
insulin response in healthy subjects. The role of rye fiber in insulin
and glucose metabolism is not known.
Objective: The aim of the study was to determine the effect of the content of rye fiber in rye breads on postprandial insulin and glucose responses.
Design: Nineteen healthy postmenopausal women aged 61 ± 1 y, with a body mass index (in kg/m2) of 26.0 ± 0.6, and with normal glucose tolerance participated in the study. The test products were refined wheat bread (control), endosperm rye bread, traditional rye bread, and high-fiber rye bread; each bread provided 50 g available carbohydrate and was served with breakfast. Plasma glucose, insulin, glucose-dependent insulinotropic polypeptide, glucagon-like peptide 1, and serum C-peptide were measured in fasting and 8 postprandial blood samples. In vitro starch hydrolysis and the microscopic structure of the breads were also determined.
Results: Postprandial insulin, glucose-dependent insulinotropic polypeptide, and C-peptide responses to the rye breads were significantly lower than the response to the control; no significant differences in insulin and C-peptide responses to the rye breads were found. Glucose and glucagon-like peptide 1 responses to the rye breads were not significantly different from those to the control, except at 150 and 180 min. In vitro starch hydrolysis was slower in all rye breads than in the control, and the structure of continuous matrix and starch granules differed between the rye and control breads.
Conclusion: Total fiber content does not explain the lower postprandial insulin response to rye bread than to wheat bread, but structural differences between rye and wheat breads might.
Key Words: Rye • wheat • cereal fiber • postprandial • blood glucose • insulin • C-peptide • glucose-dependent insulinotropic polypeptide • glucagon-like peptide 1 • postmenopausal women
INTRODUCTION
The Western-type, carbohydrate-rich diet—which involves
frequent snacking—leads to continuous pancreatic stimulation
and repeated postprandial excursions of insulin. This type of
diet has been hypothesized to predispose to insulin resistance,ß-cell dysfunction, and ultimately type 2 diabetes (1). A low-glycemic index diet that is high in fiber and whole-grain cereal
products results in decreases in postprandial insulin and glucose responses, which is thought to be beneficial to insulin and
glucose metabolism (2).
We showed previously that whole-meal rye bread and rye bread baked with whole kernels produce a lower insulin response than does refined wheat bread but no differences in glucose responses in healthy subjects (3, 4). These findings suggest that less insulin is required for the regulation of postprandial glucose excursions after the consumption of rye breads. The differences in the fiber content and structural characteristics between the rye and wheat breads may explain this finding. In most earlier studies in healthy (5) and diabetic (6-9) persons, with breads baked with milled flour, the postprandial glucose response was not affected by the amount of cereal fiber. However, in that study, the insulin response was not determined in healthy persons (5).
Preservation of the intact botanical structure of cereal grains has also been shown to lower the insulin response (10). Furthermore, food processing, such as baking, has been shown to reduce the digestibility of starch (11), which indicates the importance of preserved food structure and resistant starch for reduced hydrolysis.
In the present study we aimed to clarify the effect of rye fiber on the postprandial insulin response by changing the fiber content in rye breads. We also sought to clarify the role that differences in the structural properties of starch granules and the bread matrix may play in determining the postprandial insulin responses to rye and wheat breads.
SUBJECTS AND METHODS
Subjects
Twenty healthy, nondiabetic, postmenopausal women
were recruited for the study. One woman discontinued the
study because of heart problems after the first visit. The basic
characteristics of the remaining 19 subjects are shown in Table
1. All but one woman had normal glucose tolerance at the time
of entry to the study, as determined by a 2-h oral-glucose-tolerance test according to World Health Organization criteria
(12). One woman had impaired fasting glucose. The subjects'
mean energy intake, calculated from a 4-d food record kept
before the first study visit, was 7213 kJ/d (1723 kcal/d). Their
body weight and intakes of energy, carbohydrates, and fiber
before each test day remained unchanged throughout the study.
The MICRO-NUTRICA software package (version 2.5; Finnish Social Insurance Institution, Turku, Finland) was used to
calculate energy and nutrient intakes. The protocol for the
study was approved by the Ethics Committee of the Kuopio
University and University Hospital.
View this table:
TABLE 1. . Characteristics of the subjects at the time of entry into the study1
Postprandial study
The subjects fasted 12-15 h before the tests. On the test
morning, body weight was measured and an intravenous catheter was inserted in the antecubital vein of the arm. After the
fasting blood sample was taken, the subjects received the test
meal, which contained the test bread (50 g available carbohydrates), 40 g cucumber, and 3 dL of a noncaloric orange drink.
Eight blood samples were taken after the start of eating (15, 30,
45, 60, 90, 120, 150, and 180 min) for the measurement of
plasma glucose, insulin, glucose-dependent insulinotropic
polypeptide (GIP), and glucagon-like peptide 1 (GLP-1), and 3
blood samples were taken after the start of eating (30, 60, and
120 min) for the measurement of serum C-peptide
concentrations.
The test bread portions were served in random order at intervals of 1-2 wk. Wheat bread (control) was served twice to reduce the intraindividual variation, and the mean of these 2 determinations was used in the statistical analysis. Eating of traditional and high-fiber rye breads took longer than that of wheat bread (P = 0.006 and P = 0.0001, respectively). On average, refined wheat bread was eaten in 7 min and 46 s, endosperm rye bread in 8 min and 24 s, traditional rye bread in 9 min and 26 s, and high-fiber rye bread in 12 min and 42 s.
The subjects were advised to maintain their diet, body weight, and other living habits. Body weight was measured at each visit, and energy intake was quantified by recording the foods eaten before each test day. Heavy exercise and unusually large portions of food were forbidden on the day before each test, as was the consumption of alcohol for 2 d before the tests. Smoking was also forbidden on the morning of each test. The subjects were asked to arrive for all 5 study visits at the laboratory by car or by bus, if possible, to avoid extra stress.
Test products
The rye breads chosen as test products were endosperm rye
bread, traditional whole-meal rye bread, and whole-meal rye
bread enriched with rye bran (high-fiber rye bread). The test
products for the postprandial study were chosen by using the in
vitro starch hydrolysis method (see below). Commercial refined wheat bread (EloPakari; Vaasan & Vaasan Oy, Kuopio,
Finland) was used as the reference (control) bread.
Sourdough containing both yeast and lactobacilli was used in all rye breads. The endosperm rye bread formula comprised commercial rye endosperm flour (900 g), sourdough (731 g), water (430 g), fresh yeast (19 g), and salt (12.9 g). Sourdough was prepared from commercial endosperm flour (380 g), L62 (0.4 g Lactobacillus brevis) L73 (0.4 g L. plantarum), fresh yeast (3.8 g), and water (632 g). Traditional rye bread formula comprised commercial whole-meal rye flour (900 g), sourdough (731 g), water (450 g), fresh yeast (19 g), and salt (12.9 g). Sourdough was prepared from whole-meal rye flour (380 g), L62 (0.4 g L. brevis), L73 (0.4 g L. plantarum), fresh yeast (3.8 g), and water (632 g). High-fiber rye bread comprised whole-meal rye flour (540 g), rye bran (390 g), sourdough (731 g), water (450 g), fresh yeast (19 g), and salt (12.9 g). The sourdough was prepared similarly to whole-meal rye bread.
The dietary fiber content of the breads was determined
according to Asp et al (13), the protein content by the Kjeldahl
method (nitrogen x 5.7), and the fat content gravimetrically by
extraction in diethyl ether and petroleum ether after hydrolysis
with acid (Association of Official Analytical Chemists method
922.06, 1995). The moisture content was determined by oven
drying at 130 °C for 1 h. The energy value (kJ) per test portion
was calculated by using the weight of the portion (g) and the
following formula:
RESULTS
Postprandial plasma glucose and insulin responses
No significant differences in glucose responses to the test
breads were observed during the first 2 h after the breads were
eaten (Figure 1).
The maximal glucose responses, the times to
reach the maximal response, and the AUCs did not differ
significantly among the breads (Table 3).
However, glucose
concentrations in response to refined wheat bread had fallen
below baseline fasting concentrations and were lower than
corresponding concentrations in response to endosperm rye
bread and to traditional rye bread at 150 and 180 min (P =
0.012-0.036) and to high-fiber rye bread at 180 min (P =
0.048) (Figure 1).
FIGURE 1. Mean fasting and postprandial glucose, insulin, C-peptide,
glucose-dependent insulinotropic polypeptide (GIP), and glucagon-like
peptide 1 (GLP-1) responses to endosperm rye (), traditional rye (),
high-fiber rye (), and refined wheat (•) breads over 180 min. For each
time point, means significantly different from the mean for refined wheat
bread are indicated by letters (a, endosperm rye bread; b, traditional rye
bread; c, high-fiber rye bread; P < 0.05, Wilcoxon's test with Bonferroni
adjustment). The pooled SEM of glucose was 0.8 for endosperm rye bread,
0.7 for traditional rye bread, 1.0 for high-fiber rye bread, and 1.0 for refined
wheat bread. The corresponding pooled SEMs for insulin were 59.6, 58.3,
74.1, and 92.3 mmol/L; those for C-peptide were 0.5, 0.4, 0.5, and 0.6
nmol/L; those for GIP were 27.5, 17.6, 18.4, and 23.7 pmol/L; and those
for GLP-1 were 16.6, 11.6, 14.1, and 13.3 pmol/L. n = 19.
View this table:
TABLE 3.. Maximal glucose, insulin, C-peptide, glucose-dependent insulinotropic polypeptide (GIP), and glucagon-like peptide 1 (GLP-1) concentrations and
areas under the curve in response to the consumption of the test breads1
Insulin responses at several time points after the consumption of all rye breads were significantly different from those
after the refined wheat bread, but there were no significant
differences between the responses of the rye breads (Figure 1).
Compared with the refined wheat bread, significantly lower
insulin responses were observed to endosperm rye bread at 30,
45, 60, and 90 min, and significantly higher responses were
observed at 180 min (P = 0.0001-0.006). Similarly, the responses to traditional rye bread at 45, 60, and 90 min (P =
0.0001-0.024) and to high-fiber rye bread at 0, 45, 60, and 90
min were lower and the response to the latter was higher at 180
min (P = 0.0001-0.030). Furthermore, the maximal insulin
responses to rye breads were lower than those to refined wheat
bread (P = 0.0001-0.006) (Table 3). Also, the postprandial
insulin AUCs were significantly smaller for endosperm and
traditional rye breads than for refined wheat bread (P = 0.0001
and P = 0.006, respectively) and the AUC was nearly significantly smaller for high-fiber rye bread (P = 0.06). The time
intervals to reach the maximal insulin response did not differ
significantly in any comparison among the test breads.
Postprandial serum C-peptide responses
The serum C-peptide responses mirrored the insulin responses (Figure 1). Responses to endosperm rye and high-fiber
rye breads at 30 and 60 min (P = 0.0001-0.036) and to
traditional rye bread at 60 min (P = 0.0001) were lower than
those to refined wheat bread. In addition, the maximal C-peptide responses (P = 0.0001-0.006) and the 120-min AUC
to all rye breads (P = 0.006 for all breads) were smaller than
those to wheat bread (Table 3). No significant differences
among the breads in the time interval to reach the maximal
C-peptide responses were seen.
Postprandial plasma GIP and GLP-1 responses
The plasma GIP responses to rye breads were significantly
lower than those to wheat bread at several time points: for
endosperm rye bread at 60 and 90 min (P = 0.0001 and P =
0.018, respectively); for traditional rye bread at 30, 45, 60, 90,
and 120 min (P = 0.0001-0.006); and for high-fiber rye bread
at 30, 45, 60, and 90 min (P = 0.0001-0.006) (Figure 1). In
addition, the GIP responses to endosperm rye bread were
higher than those to traditional rye bread at 30 and 60 min and
to high-fiber rye bread at 30, 45, and 60 min (P =
0.006-0.042).
Furthermore, the maximal GIP increases after traditional and high-fiber rye breads were significantly smaller than the increase after wheat bread (P = 0.0001 and P = 0.0001, respectively), as were the AUCs for all rye breads (P = 0.0001-0.036) (Table 3). Also, the maximal responses to traditional rye and high-fiber rye breads (P = 0.012 and P = 0.030, respectively) and the AUC for traditional rye bread (P = 0.024) were smaller than the corresponding values for endosperm rye bread (Table 3).
No significant differences were found in the GLP-1 responses among the test breads, except at the end of the study between the high-fiber rye bread and wheat bread (P = 0.012 at 150 min and P = 0.012 at 180 min) (Figure 1). The maximal increases, maximal times, and the AUCs for GLP-1 also did not differ significantly among the test products (Table 3).
In one of the subjects the GIP and GLP-1 responses did not rise above the fasting concentration during the first postprandial test for refined wheat bread. The AUCs for GIP and GLP-1 calculated from the second postprandial test with refined wheat bread were therefore used as the mean values of the responses to wheat bread in this subject. The statistical analyses were also repeated after this subject's data were eliminated from the analyses, but the results remained essentially unchanged.
In vitro starch hydrolysis
In vitro starch hydrolysis differed among the test breads
(P = 0.029; Figure 2). Hydrolysis indexes of 82 ± 3, 76 ± 2,
and 71 ± 4 were obtained for the endosperm, traditional, and
high-fiber rye breads, respectively.
FIGURE 2. Rate of starch hydrolysis after endosperm rye bread (),
traditional rye bread (), high-fiber rye bread (), and refined wheat bread
() were chewed, incubated with pepsin, and subsequently incubated with
pancreatic -amylase in a dialysis tube.
Microscopy of the breads
The structure of starch granules and the continuous matrix
between the starch granules were very different between the
wheat and rye breads. In wheat bread, green-stained protein
(gluten) formed a continuous matrix in which starch granules
were dispersed (Figure 3A). In rye breads, starch granules
were swollen, and amylose had partly leached out (Figure 3, B-D). The starch granules were also closely packed and
formed a continuous matrix. The softness and porousness of
refined wheat bread and the hardness of rye breads are based on
these structural differences between rye and wheat breads.
FIGURE 3. Light micrographs of refined wheat bread (A), endosperm rye bread (B), high-fiber rye bread (C), and traditional rye bread (D). Protein
appears green, amylopectin starch appears brown to gray, and amylose starch appears blue. Protein (gluten, stained green) makes the refined wheat bread
soft, whereas the highly swollen starch granules and outleached amylose starch make the rye bread hard.
DISCUSSION
The present study confirmed our previous findings that, in
healthy subjects, less insulin is needed for the control of
postprandial glucose excursions after the ingestion of rye bread
than after the ingestion of refined wheat bread and that a lower
insulin response is associated with parallel changes in plasma
GIP (3, 4). Furthermore, we also showed that the lower insulin
response after rye bread is not explained by the amount of fiber
in rye bread. The lower C-peptide response after ingestion of
rye bread indicates that the diminished pancreatic secretion of
insulin rather than enhanced liver extraction contributes to the
lower insulin response. Our study was tightly controlled by
design and dietary and lifestyle factors to minimize the possible
confounding effects; therefore, our study offers convincing
evidence of the beneficial effect of rye bread on insulin metabolism, at least acutely. Importantly, the intake of energy
during the day preceding each postprandial experiment and the
body weights of the study subjects did not change during the
study.
In agreement with previous findings (5-9), the postprandial glucose response in the present study was unaffected by the content of fiber in the breads. Even though the glucose responses did not initially differ quantitatively, wheat bread was characterized by a decrease in glucose below fasting concentrations at the tail of the curve between 2 and 3 h. These decreased circulating glucose concentrations postprandially may increase hunger, increase the drive to eat, and stimulate the release of counterregulatory hormones (21). We also found smaller hydrolysis indexes for the rye breads (index: 71-82) than for wheat bread (index: 100) in vitro, which indicates a slower hydrolysis of starch in rye products. The findings of our postprandial study suggest that plasma glucose is tightly regulated in healthy persons, and possible differences in the release of glucose from different cereals are observed only as parallel changes in the demand of insulin. However, the fact that peripheral blood glucose represents the net effect of many postabsorptive processes in addition to the rate of glucose absorption should not be overlooked (22).
The insoluble components of cereal fibers are known to be ineffective in the regulation of postprandial glycemia and insulinemia when ingested with a glucose load (23, 24), although the role of insoluble cereal fiber in bread has not been well studied. Rye fiber also contains soluble fiber in the form of arabinoxylan (9%) and ß-glucan (2-3%) (25, 26). In the present study, however, the amount of soluble fiber in rye bread portions was small (3.0-4.8 g/portion), although it was greater than in refined wheat bread (1.2 g/portion). Furthermore, the absolute difference between the wheat and endosperm rye breads was as great as was the difference between endosperm and high-fiber rye bread. In earlier studies that showed a decrease in both the insulin and the glucose responses with arabinoxylan-enriched wheat breads and ß-glucan-rich barley breads, the content of soluble fiber was considerably larger, ranging from 3.7 to 14.1 g/portion (27, 28).
The reduced insulin response after the rye breads may also have been due to larger portions and longer ingestion times after traditional rye bread and high-fiber rye bread than after ingestion of wheat bread. This is not likely, however, because the portions and eating times for wheat and endosperm rye breads were almost identical, and the insulin responses between the endosperm and traditional, or the endosperm and high-fiber rye breads, did not differ significantly. There were also small differences in the fat and protein contents of the test bread portions. Although both nutrients are known to affect postprandial glucose and insulin responses (29, 30), findings with starchy foods (bread, spaghetti, and rice) (5) and with mixed meals (31) have shown that small differences in the intake of these nutrients have negligible effects on the overall postprandial glucose and insulin responses.
Incretins are hormones that are secreted during meals and that potentiate the insulin response to levels above those observed when the corresponding stimulus (usually glucose) is administered intravenously (32). The most important insulinotrophic incretins are GLP-1 and GIP. It is possible that the lower insulin response after rye bread in the present study was in part mediated by GIP. However, our previous intervention study showed that the first-phase insulin response to intravenous glucose was enhanced by 8 wk of rye bread ingestion as compared with ingestion of refined wheat bread (33). Because the response to intravenous glucose bypasses the gut incretin effect, the lowered postprandial insulin response to rye bread may not be solely explained by the reduced GIP response. On the other hand, different mechanisms may explain the decreased response of GIP to rye bread. Soluble fibers, such as guar gum, have been shown to decrease postprandial insulin and GIP responses in healthy persons (34-36) and in persons with type 2 diabetes (36, 37)—with one exception (38)—whereas insoluble fiber in the form of wheat bran (34) or cellulose (39) showed no effect. Also, the food structure may have an influence on GIP, but no studies regarding the role of mechanical food structure in the release of incretin have been published.
Because the present results on postprandial insulin responses are unlikely to be explained by the amount of dietary insoluble or soluble fiber, there may be other relevant differences between the wheat and rye breads. The structures of the continuous matrix and starch granules differed between rye and wheat breads after baking. In rye bread, a continuous phase was formed by closely packed starch granules, whereas in wheat bread the starch granules were entrapped in an extensible gluten network that formed the continuous phase. This caused a less porous and mechanically firmer structure in rye breads (40). Therefore, particle size before swallowing was probably much higher for rye than for wheat breads and could explain the slower rate of hydrolysis found in this study and previously (41). Furthermore, in wheat bread, starch remained inside the granule, became gelatinized, and was more accessible to hydrolysis by amylolytic enzymes. In contrast, in rye breads, amylose leached out and coated the starch granules, which made the starch resistant to hydrolysis after cooling. This phenomenon has been reported previously in rye bread (42). The coating of amylose on the surface of starch granules has also been suggested to retard the hydrolysis of amylopectin, the other main constituent of starch (43). In addition, the endogenous arabinoxylan-degrading enzyme xylanase in rye flour contributes to the release of amylose from starch granules (16).
The present study showed that a lower insulin secretion after the ingestion of rye bread than after the ingestion of wheat bread is not explained by the quantity of rye fiber in the bread but may be explained by differences in the structural properties of the 2 breads.
ACKNOWLEDGMENTS
We thank Kati Katina for baking the test breads, Eeva Lajunen for
technical and laboratory assistance, and Sebastiaan Bol for assistance with
the calculations of the AUCs.
KSJ wrote the first draft of the manuscript. All of the authors contributed to the revisions and subsequent drafts and reviewed the final version of the manuscript. None of the authors had any financial or personal relationship with sponsors of this work.
REFERENCES